Nitric oxide insufficiency, platelet activation, and arterial thrombosis

Circulation Research

Volumn 88, Issue 8, 2001, Pages 756-762

  Loscalzo, Joseph ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Endothelium; Nitric oxide synthase; Nitroglycerin; Oxidative stress; S nitrosothiols

Indexed keywords

ANTIOXIDANT; CALCIUM ION; CYCLOOXYGENASE 1; GLUTATHIONE PEROXIDASE; GUANYLATE CYCLASE; HYDROGEN; LIPID PEROXIDASE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PHOSPHATIDYLINOSITOL 3 KINASE; REACTIVE OXYGEN METABOLITE;

ARTERY THROMBOSIS; CALCIUM TRANSPORT; CATALYSIS; ENDOTHELIUM LESION; ENZYME ACTIVATION; ENZYME INHIBITION; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PRIORITY JOURNAL; REDUCTION; REVIEW; THROMBOCYTE ACTIVATION; THROMBOCYTE ADHESION; THROMBOCYTE AGGREGATION; VASODILATATION;

EID: 0035957630     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/hh0801.089861     Document Type: Review

References (83)

1. Furchgott RF, Zawadzki JV. The obligatory role of endothetial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature. 1988;245: 524-530.
2. Hampton JR, Harrison AJ, Honour AJ, Mitchell JR. Platelet behavior and drugs used in cardiovascular disease. Cardiovasc Res. 1967;1:101-106.
3. Needleman P, Jakschik B, Johnson ME. Sulfhydryl requirement for relaxation of vascular smooth muscle. J Pharm Exp Ther. 1973;187: 324-331.
4. Katsuki S, Arnold W, Mittal C, Murad F. Stimulation of guanylate cyclase by sodium nitropursside, nitroglycerin and nitric oxide in various tissue preparations and comparison to the effects of sodium azide and hydroxylamine. J Cyclic Nucleotide Res. 1977;3:23-35.
5. Mellion BJ, Ignarro LJ, Ohlstein EH, Pontecoruo EG, Hyman AL, Kadowitz PJ. Evidence for the inhibitory role of guanosine 3′,5′-monophosphate in ADP-induced human platelet aggregation in the presence of nitric oxide and related vasodilators. Blood. 1983;57:946-955.
6. Loscalzo J. N-Acetylcysteine potentiates inhibition of platelet aggregation by nitroglycerin J Clin Invest. 1985;76:703-708.
7. Cunningham M, Loscalzo J. Nitroprusside can induce clinically important platelet dysfunction only detectable in vitro by incubation with reduced thiol. Clin Res. 1985;33:337A.
8. Stamler J, Cunningham M. Loscalzo J. Reduced thiols and the effect of intravenous nitroglycerin on platelet aggregation. Am J Cardiol. 1988;62: 377-380.
9. Folts JD. Stamler J. Loscalzo J. Intravenous nitroglycerin infusion inhibits cyclic blood flow responses caused by periodic platelet thrombus formation in stenosed canine coronary arteries. Circulation. 1991;83:2122-2127.
10. Stamler JS, Loscalzo J. The antiplatelet effects of organic nitrates and related nitroso compounds in vitro and in vivo and their relevance to cardiovascular disorders. J Am Coll Cardiol. 1991;18:1529-1536. Abstract.
11. Horowitz JD. Nitrovasodilators. In: Loscalzo J, Vita JA, eds. Nitric Oxide and the Cardiovascular System. Totowa, NJ: Humana Press; 2000:383-409.
12. Ignarro LJ, Byms RE, Buga GM, Wood KS. Endothelium-derived relaxing factor from pulmonary artery and vein possesses pharmacologic and chemical properties identical to those of nitric oxide radical. Circ Res. 1987; 61:P866-P879.
13. Palmer RMJ, Ferrige AG, Moncada S. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature. 1987;327: 524-526.
14. Azuma H, Ishikawa M, Sekizaki S. Endotheliuni-dependent inhibition of platelet aggregation. Br J Pharmacol. 1986;88:411-415.
15. Radomski MW, Palmer RMJ, Moncada S. Comparative pharmacology of endothelium-derived relaxing factor, nitric oxide, and prostacyclin in platelets. Br J Pharmacol. 1987;92:181-187.
16. Stamler JS, Singel DJ, Loscalzo J. Biochemistry of nitric oxide and its redox-active forms. Science. 1992;258:1898-1902.
17. Kelm M. Nitric oxide metabolism and breakdown. Biochim Biophys Acta. 1999;1411:273-289.
18. Stamler JS, Jaraki O, Osborne J, Simon D I, Keaney J, Vita J, Singel D, Valeri CR, Loscalzo J. Nitric oxide circulates in mammalian plasma primarily as an S-nitroso adduct of serum albumin. Proc Natl Acad Sci U S A. 1992;89:7674-7677.
19. Scharfstein JS, Keaney JF Jr, Slivka A, Welch GN, Vita JA, Stamler JS, Loscalzo J. In vivo transfer of nitric oxide between a plasma protein-bound reservoir and low molecular weight thiols. J Clin Invest. 1994;94:1432-1439.
20. Liu GZ, Rudd MA, Freedman JE, Loscalzo J. S-transnitrosation reactions are involved in the metabolic fate and biological actions of nitric oxide. J Pharmacol Exp Ther. 1998;284:526-534.
21. Hirayama A, Noronha-Dutra AA, Gordge MP, Neild GH, Hothersall JS. S-nitrosothiols are stored by platelets and released during platelet-neotraphil interactions. Nitric Oxide. 1999;3:95-104.
22. Stamler J, Mendelsohn ME, Amarante P. Smick D, Andon N, Davies PF, Cooke JP, Loscalzo J. N-Acetylcysteine potentiates platelet inhibition by endothelium-derived nitric oxide. Circ Res. 1989;65:789-795.
23. Mendelsohn ME, O'Neill S, George D, Loscalzo J. Inhibition of fibrinogen binding to human platelets by S-nitroso-N-aeetylcysteine. J Biol Chem. 1990; 265:19028-19034.
24. Michelson AD, Benoit SE, Furman MI, Breckwoldt WL, Rohrer MJ, Barnard MR, Loscalzo J. Effects of nitric oxide/EDRF on platelet surface glycoproteins. Am J Physiol. 1996;39:H1640-H1648.
25. 2+ stores. Circ Res. 1999; 84:205-209.
26. Ptasznik A, Traynor-Kaplan A, Bokoch G. G protein-coupled chemoattractant receptors regulate Lyn tyrosine kinase Shc adapter protein signaling complexes. J Biol Chem. 1995:270:19969-19973.
27. Kucera G, Rittenhouse S. Human platelets form 3-phosphorylated phosphoinositides in response to α-thrombin, U46619, or GTPγS. J Biol Chem. 1990;265:5345-5348.
28. Yanagi S, Sada Y, Tohyama Y, Tsubokawa M, Nagai K, Yonezawa K, Yarnamura H. Translocation, activation and association of protein-tyrosine kinase (p72syk) with phosphoinositide 3-kinase and early events during platelet activation. Eur J Biochem. 1994;224:329-333.
29. Kurosu H, Maehama T, Okada T, Yamamoto T, Hoshino S, Fukui Y, Ui M, Hazeki O, Katada T. Heterodimeric phosphoinositide 3-kinase consisting of p85 and p110β is synergistically activated by the β-γ subunits of G proteins and phosphotyrosyl peptide. J Biol Chem. 1997;272:24252-24256.
30. Hazeki O, Okada T, Kuorsu H, Takasuga S. Suzuki T, Katada T. Activation of PI 3-kinase by G protein β-γ subunits. Life Sci. 1998;62:1555-1559.
31. Zhang J, Shattil SJ, Cunningham M, Rittenhouse S. Phosphoinositide 3-kinase γ and p85/phosphoinositide 3-kinase in platelets: relative activation by thrombin receptor or β-phorbol myristate acetate and roles in promoting the ligand binding function of αIIbβ3 integrin. J Biol Chem. 1996;271: 6265-6272.
32. 1 and nitroglycerin. Circ Res. 1989;65:796-804.
33. Pigazzi A, Heydrick S, Folli F, Benoit S, Michelson AD, Loscalzo J. Nitric oxide inhibits thrombin receptor-activating peptide-indueed phosphoinositide 3-kinase activity in human platelets. J Biol Chem. 1999;274:14368-14375.
34. Banfic H, Downes CP, Rittenhouse SE. Biphasic activation of PKBα/Akt in platelets: evidence for stimulation both by phosphatidylinositol 3,4bisphosphate, produced via a novel pathway, and by phosphatidylinositol 3,4,5-triphosphate. J Biol Chem. 1998;273:11630-11637.
35. Majka M, Ratajczak J, Kowalska MA, Ratajczak MZ. Binding of stromal derived factor-1α (SDF-1 α) to CSCR4 chemokine receptor in normal human megakaryoblasts but not in platelets induces phosphorylation of mitogen-activated protein kinase p42/44 (MAPK), ELK-1 transcription factor and serine/ threonine kinase Akt, Eur J Haenmatol. 2000;64:164-172.
36. Radomski MW, Palmer RMJ, Moncada S. Endogenous nitric oxide inhibits human platelet adhesion in vascular endothelium. Lancet. 1987;2:1057-1058,
37. Inbal A, Gurevitz O, Tamarin I, Eskaraev R, Chetrit A, Novicov I, Feldman M, Varon D, Eldar M. Loscalzo J. Unique antiplatelet effects of a novel S-nitrosoderivalive of a recombinant fragment of von Willebrand factor, AR545C: in vitro and ex vivo inhibition of platelet function. Blood. 1999; 94:1693-1700.
38. Gurevitz. O, Skutelsky E, Eldar M. Tamarin I, Shenkrnan B, Eskaraev R, Varon D, Loscalzo J, Inbal A. S-nitrosoderivative of a recombinant fragment of von Willebrand factor (5-nitfoso-AR545C) inhibits thrombus formation in guinea pig carotid artery thrombosis model. Thromb Haemostat 2000;84: 912-916.
39. Wu CC, Ko FN, Teng CM. Inhibition of platelet adhesion to collagen by cGMP-elevating agents. Biochem Biophys Res Commun. 1997;231:412-416.
40. Marks DS, Vita JA, Foils JD, Keaney JF Jr. Welch GN, Loscalzo J. Inhibition of neointimal proliferation in rabbits after vascular injury by a single treatment with a protein adduct of nitric oxide. J Clin Invest. 1995;96: 2630-2638.
41. Kader KM, Akella R, Ziats NP, Lakey LA, Harasaki H, Ranieri JP, Bellamkonda RV. eNOS-overexpressing endothelial cells inhibit platelet aggregation and smooth muscle proliferation in vitro. Tissue Eng. 2000;6:241-251.
42. Fujimoto Y, Tagano S, Ogawa K, Sakuma S, Fujita T. Comparison of the effects of nitric oxide and peroxynitrite on the 12-lipoxygenase and cyclooxygenase metabolism of arachidonic acid in rabbit platelets. Prostaglandins Leukot Essent Fatty Acids. 1998;59:95-100.
43. Boulos C, Jiang H, Balazy M. Diffusion of peroxynitrite into the human platelet inhibits cyclooxygenase via nitration of tyrosine residues. J Pharmacol Exp Ther. 2000;293:222-229.
44. Megson IL, Sogo N, Mazzei FA, Butler AR, Wallon JC, Webb DJ. Inhibition of human platelet aggregation by a novel S-nitrosothiol is abolished by haemoglobin and red blood cells in vitro: implications for antii-thrombotic therapy. Br J Pharmacol. 2000;131:1391-1398.
45. Folts JD. An in vivo model of experimental arterial stenosis, intimal damage, and periodic thrombosis. Circulation. 1991;83(suppl IV):3-14.
46. Keaney JF Jr, Stamler JS, Scharftslein J, Folts JD, Loscalzo J. Nitric oxide forms a stable adduct with serum albumin that has potent antiplatelet properties in vivo. Clin Res. 1992:40:194A. Abstract.
47. Zai A, Rudd MA, Scribner AW, Loscalzo J. Cell-surface protein disulfide isomerase catalyses transnitrosation and regulates intracellular transfer of nitric oxide. J Clin Invest. 1999;103:393-399.
48. Langford EJ, Brown AS, Wainwright RJ, de Belder AJ, Thomas MR, Smith RE, Radomski MW, Martin JF, Moncada S. Inhibition of platelet activity by S-nitrosoglutathione during coronary angioplasty. Lancet. 1994;344: 1458-1460.
49. Nong Z, Hoylaerts M, Van Pelt N, Collen D, Janssens S. Nitric oxide inhalation inhibits platelet aggregation and platelet-mediated pulmonary thrombosis in rats. Cric Res. 1997;81:865-869.
50. Simon DI, Stamler JS, Loh E, Loscalzo J, Francis SA, Creager MA, Effect of nitric oxide synthase inhibition on bleeding time in humans. J Cardiovasc Pharmacol. 1995;26:339-342.
51. Maalej N, Albrecht R, Losealzo J, Folts JD. The potent platelet inhibitory effects of S-nitiosated albumin coating of artificial surfaces, J Am Coll Cardiol. 1999;33:1408-1414.
52. Annich GM, Meinhardt JP, Mowery KA, Ashlotn BA, Merz SI, Hirschl RB, Meyerhoff ME, Bartlett RH. Reduced platelet activation and thrombosis in extraeorporeal circuits coated with nitric oxide release polymers. Crit Care Med. 2000;28:915-920.
53. Cooke JP, Stamler J, Andon N, Davies PF, McKinley G, Loscalzo J. Flow stimulates endothelial cells to release a nitrovasoditator that is potentiated by reduced thiol. Am J Physiol. 1990;28:H804-H812.
54. Sase K, Michel T, Expression of constitutive endothelial nitric oxide symhase in human blood platelets. Life Sci. 1995;57:2049-2055.
55. Pigazzi A, Fabian A, Johnson J, Upchurch GR, Loscalzo J. Identification of nitric oxide synthases in human megakaryocytes and platelets. Circulation. 1995;92:I-365.
56. Zhou Q, Hellermann GR, Solomonson LP. Nitric oxide release from resting human platelets. Thromb Res. 1995;77:87-96.
57. Freedman JE, Loscalzo J. Barnard MR, Alpert C, Keaney JF Jr, Michelson AD. Nitric oxide release from activated platelets inhibits platelet recruitment. J Clin lnvest. 1997;100:350-356.
58. Freedman JE, Sauter R, Battinelli EM, Ault K, Knowles C, Huang PL, Loscalzo J. Deficient platelet-derived nitric oxide and enhanced hemostasis in mice lacking the NOSIII gene. Circ Res. 1999;84:1416-1421.
59. Freedman JF., Li L, Sauter R. Keaney JF Jr. α-Tocopherol and protein kinase C inhibition enhance platelet-derived nitric oxide. FASEB J. 2000;14: 2377-2379.
60. Freedmars JE. Farhat JH, Loscalzo J, Keaney JF Jr. α-Toeopherol inhibits aggregation of human platelets by a protein kinase C-dependenl mechanism. Circulation. 1996;94:2434-2440.
61. Laufs U, Gertz K, Huang P, Nickenig G, Bohn M, Dimagl U, Endres M. Atorvastatin upregulates type III nitric oxide synthase in thrombocytes, decreases platelet activation, and protects from cerebral ischemia in nonmocholesterolemic mice. Stroke. 2000;31:2442-2449.
62. Laufs U, Fata VL, Plutzky J, Liao JK, Upregulation of endothelial nitric oxide synthase by HMG CoA reductase inhibitors. Circulation. 1998;97: 1129-1135.
63. Anfossi G, Russo I, Massucco P, Mattiello L, Perna P, Tasssone F, Trovati M. L-arginine modulates aggregation and intraceltular cyclic 3,5-guanosine monophosphate levels in human platelets: direct effect and interplay with anlioxidative thiol agent. Theomb Res. 1999;94:307-316.
64. Chen L, Salafranca MN, Mehta JL,Cyclooxygenase inhibition decreases nitric oxide synthase activity in human platelets. Am J Physiol. 1997;273: H1854-H1859.
65. Ikeda H, Takajo Y, Murohara T, Ichiki K, Adachi H, Haramaki N, Katoh A, Imaizumi T, Platelet-derived nitric oxide and coronary risk factors. Hypertension. 2000;35:904-907.
66. Ichiki K, Ikeda H, Haramaki N, Ueno T, Imaizumi T, Long-term smoking impairs platelet-derived nitric oxide release. Circulation. 1996;94: 3109-3114.
67. Freedman JE, Ting B, Hankin B, Loscalzo J, Keaney JF, Jr, Vita JA. Impaired platelet production of nitric oxide predicts presence of acute coronary syndromes. Circulation. 1998;98:1481-1486.
68. Freedman JE, Loscalzo J, Benoit SE, Valeri CR, Barnard MR, Michelson AD. Decreased platelet inhibition by nitric oxide in two brothers with a history or arterial thrombosis. J Clin Invest. 1996;97:979-987.
69. Maddipati KR, Gasparski C, Marnett LJ. Characterization of the hydroperoxide-reducing activity of human plasma. Arch Biochem Biophys. 1987;254:9-17.
70. Maddipati KR, Marnett LJ. Characterization of the major hydroperoxide reducing activity of human plasma. J. Biol Chem. 1987;262:17398-17403.
71. Freedman JE, Frei B, Welch GN, Loscalzo J. Glutaihione peroxidase potentiates the inhibition of platelet function by S-nitrosothiols. J Clin Invest. 1995;96:394-400.
72. Rubbo H, Radi R, Trujillo M, Telleri R, Kalyanaraman B, Barnes S, Kirk M, Freeman BA. Nitric oxide regulation of Superoxide arid peroxymtrite dependent lipid peroxidation: formation of novel nitrogen-containing oxidized lipid derivatives. J. Biol Chem. 1994;269:26066-26075.
73. Jahn B, Hansch GM. oxygen radical generation in human platelets: dependence on 12-lipoxygenase activity and on the glutathione cycle, Int Arch Allergy Immunol. 1990;93:73-79.
74. Kenet G, Freedman J, Shenkman B, Regina E, Brok-Simoni F, Holzman F, Vavva F, Brand N, Michelson A, Trolliet M, Loscalzo J, Inbal A, Plasma glutathione peroxidase deficiency and platelet insensitivity to nitric oxide in children with familial stroke. Arterioscler Thromb Vasc Biol, 1999;19: 2017-2023.
75. Chambers I. Frarnpton J, Goldfafb P, Affara N, McBain W, Harrison PR, The structure of the mouse glutathione peroxidase gene: the selenocysteine in the active site is encoded by the termination codon, TGA. EMBO J. 1986,5: 1221-1227,
76. Shen Q, Chu FF, Newburger PE, Sequences in the 3′-untranslated region of the human cellular glutathione peroxidase gene are necessary and sufficient for selenocysteine incorporation at the UGA codon. J Biol Chem. 1993;268: 11463-11469.
77. Voetsch B, Bierl C, Damasceno BP, Annichino-Bizzacchi JM, Arruda VR, Loscalzo J. A novel promoter polymorphism in the plasma glutathione peroxidase gene associated with arterial ischemic stroke in the young. Circulation. 2000;102:II-704.
78. Stagliano NE, Zhao W, Prado R, Dewanjee MK, Ginsberg MD, Dietrich WD, The effect of nitric oxide synthasc inhibition on acute platelet accumulation and hemodynamic depression in a rat model of thromboembolic stroke. J Cereb Blood Flow Metab. 1997;17:1182-1190.
79. Ricetta MM, Guidi GC, Tecchio C, Bellisola G, Rigo A, Perona G, Effects of sodium selenite on in vitro interactions between platelets and endothelial cells. Int J Clin Lab Res. 1999;29:80-84.
80. 2 increases platelet adhesion and reduces the antiadhesive and antiaggregatory effects of NO. Arterioscler Thromb Vasc Biol 1998;18:1248-1256.
81. Zalba G, Beaumont J, San Jose G, Fortune MA, Fortuna MA, Diez J. Vascular oxidant stress: molecular mechanisms and pathophystological implications. J Physiol Biochem. 2000;56:57-64.
82. 2 synthesis in human blood platelets. FEBS Lett. 1999;442:162-166.
83. Nappi AJ, Vass E. Hydroxyl radical formation resulting from the interaction of NO and hydrogen peroxide. Biochem Biophys Acta. 1998;1380:55-63.